Volume 3 • 2015  10.

1093/conphys/cov035

Review article

Themed Issue Article: Conservation Physiology of Animal Migrations

Toward a mechanistic understanding of

animal migration: incorporating physiological
measurements in the study of animal movement
David S. Jachowski1,2,*, and Navinder J. Singh3

1Department of Forestry and Environmental Conservation, Clemson University, 258 Lehotsky Hall, Clemson, SC 29634-0310, USA
2Schoolof Life Sciences, University of KwaZulu-Natal, Durban, SA
3Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, SE-90183 Umeå, Sweden

*Corresponding author: Department of Forestry and Environmental Conservation, Clemson University, 258 Lehotsky Hall, Clemson,
SC 29634-0310, USA. Tel: +1 864 656 2138. Email: djachowski@gmail.com

Movements are a consequence of an individual’s motion and navigational capacity, internal state variables and the influence of
external environmental conditions. Although substantial advancements have been made in methods of measuring and quanti-
fying variation in motion capacity, navigational capacity and external environmental parameters in recent decades, the role of
internal state in animal migration (and in movement in general) is comparatively little studied. Recent studies of animal move-
ment in the wild illustrate how direct physiological measurements can improve our understanding of the mechanisms underly-
ing movement decisions. In this review, we synthesize and provide examples of how recent technical advances in the
physiology-related fields of energetics, nutrition, endocrinology, immunology and ecotoxicology provide opportunities for
direct measurements of physiological state in the study of animal movement. We then propose a framework for practitioners to
enable better integration of studies of physiological state into animal movement ecology by assessing the mechanistic role
played by physiology as both a driver and a modulator of movement. Finally, we highlight the current limitations and research
priorities for better integration of direct measurements of animal physiological state into the study of animal movement.

Key words: Endocrinology, energetics, immunology, migration, movement, nutrition

Editor: Steven Cooke
Received 19 March 2015; Revised 15 June 2015; accepted 4 July 2015
Cite as: Jachowski DS, Singh NJ (2015) Toward a mechanistic understanding of animal migration: incorporating physiological measurements in
the study of animal movement. Conserv Physiol 3: doi:10.1093/conphys/cov035.

Introduction ongoing, rapid global change is shifting patterns of species

Animals move to fulfil their basic biological goals of gaining
energy, increasing survival and reproductive advantage
(Nathan et al., 2008). However, their motivation to move is
determined by a combination of internal state and external
environmental factors, such as climate, predation risk, compe-
tition and food availability (Fryxell and Sinclair, 1988). The
movements, their interactions and adaptive abilities, thereby
affecting their m
­ otivation to move (Lundberg and Moberg,
2003; Pulido, 2007; Singh et al., 2010). These changes are
challenging our abilities to understand and predict animal
movements, particularly as they relate to the process of migra-
tion, which can be defined broadly as the seasonal movement
toward non-overlapping areas (Wilcove and Wikelski, 2008).

© The Author 2015. Published by Oxford University Press and the Society for Experimental Biology. 1
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Review article
Therefore, to provide better prediction of how migratory ani-
mals will respond to global change, it is vital to develop a
more complete understanding of the relative role of internal
vs. external drivers of animal movement (Bowlin et al., 2010;
Lennox et al., 2015).
The internal state of an animal is recognized as a central
component of movement ecology in addressing the question
of why animals move (Nathan et al., 2008). However, only
recently have movement ecologists begun to clarify and
emphasize the role of internal state in observed movement
behaviours (Patterson et al., 2008). Recent rapid technical and
analytical advances in the monitoring of moving animals and
quantification of their movements have resulted in a variety of
movement models inferring behavioural responses to internal
state based on the location of successive locational fixes
(Morales et  al., 2004; Schick et  al., 2008). However, such
inferential models are indirect, and the causal mechanisms
behind these observed movement paths remain relatively
unknown (Getz and Saltz, 2008; Holyoak et al., 2008). To
date, a majority of the work describing how directly observed
changes in the internal state of animals influence movements
is restricted to captive animals exposed to different controlled,
experimental manipulations (Meier et  al., 1965; Wingfield
et al., 1990; Ward et al., 2002).
Recent studies that have attempted to directly measure the
internal state of moving, free-ranging vertebrate animals in the
wild have revealed intricate linkages between an individual’s
internal physiological state and movement. For example, the
use of biologging techniques has greatly advanced our under-
standing of animal movement over the last two decades by pro-
viding the opportunity to link expenditure and conservation of
energy with movement behaviour (Urban et al., 2007; Shepard
et al., 2009; Bogard et al., 2010; Louzao et al., 2014). Likewise,
integration of endocrine system function with animal tracking
through non-invasive stress hormone measurements has
resulted in an improved understanding of complex movement
behaviours, such as refuge use and corridor streaking
(Jachowski et al., 2012, 2013a). Collectively, there is a growing
body of evidence illustrating how internal state interacts with,
and sometimes overrides, the more commonly assessed role of
external factors used to explain observed movement behav-
iours. Perhaps most importantly, through measurements of
internal state, we are beginning to access the mechanisms
underlying animal movement (Cooke et al., 2012).
As technical developments progress and more studies
attempt to address questions about internal state and its role in
animal movement, it becomes important to review the status of
the field and identify future directions. In this special issue,
Lennox et al., 2015 discuss how physiology has improved our
understanding of animal migration and can inform conserva-
tion. In our review, we focus on providing a synthetic summary
of the tools and techniques that can be used to measure the
physiological state of moving animals. We also provide a con-
ceptual framework for how measures of physiological state
can be better integrated into studies of animal movement.
2
Conservation Physiology • Volume 3 2015
Finally, we describe limitations of the ­physiological data
­currently being obtained and used to answer questions on ani-
mal movements, and identify future research opportunities.
Throughout our review, because migration is composed of a
diversity of movement behaviours, such as nomadic move-
ments within seasonal ranges or restricted movement at a spe-
cific feeding patch (Sawyer and Kauffman, 2011; Singh and
Ericsson, 2014), we use the terms movements and migration
simultaneously because most of our arguments apply to all
types of movements in general and not only migration.
Review of techniques for measure-
ment of the physiological state of
moving animals
When attempted, the incorporation of multiple subdisciplines
of physiology has informed our understanding of animal
movement ecology. These subdisciplines primarily include
studies of animal energetics, nutrition, endocrinology, immu-
nology and ecotoxicology. Each of these fields has been exten-
sively investigated in a laboratory setting, and concepts and
methods are increasingly being applied to free-living animals
in a field setting. Our purpose here is briefly to review how
measures derived from each of these fields have informed our
study of animal movement.
Energetics
The study of energetics is fundamental to understanding pro-
cesses such as reproduction, behavioural interactions and
movement behaviour (Schmidt-Nielsen, 1997; Isaac et  al.,
2012). The rapidly advancing field of ecological energetics is of
particular relevance to movement ecologists because of its focus
on free-ranging organisms and its aim to integrate physiological
limits of an organism with the external, environmental con-
straints surrounding it (Tomlinson et al., 2014). Within a move-
ment ecology context, attention is typically focused on the
energetic costs or benefits of various movement decisions; for
example, tracking studies of invertebrate and avian movement
have revealed correlations between migratory movements and
periods of favourable wind speed and direction that are prob-
ably based on derived energetic benefits (Wikelski et al., 2006).
Also, a number of direct measures are available to assess meta-
bolic rates during movement, including changes in isotope lev-
els and direct measurements of body temperature and heart rate
through biotelemetry (Nagy and Costa, 1980; Speakman,
1997), both of which are discussed below in further detail.
Isotopes
The isotope method measures energy expenditure and water
turnover rate through the technique of doubly labelled water
(DLW). The technique relies on the extent to which an organ-
ism loses heavy oxygen isotopes (18O) in the form of carbon
dioxide and water, in relationship to the loss of heavy hydro-
gen isotopes (2H or 3H) in the form of water. The resulting
difference between the hydrogen and oxygen isotope turnover
Conservation Physiology • Volume 3 2015
rate indicates CO2 production and therefore metabolic rate
and energetic requirements (Speakman, 1997). However, there
are several assumptions behind the DLW technique that are
not always met, thus restricting its use in some taxa, such as
amphibians, diving birds and mammals, and organisms of
small body size (Speakman, 2005; Hambly and Voigt, 2011;
Shaffer, 2011). Furthermore, the 18O isotope is expensive to
procure, and the cost of this analysis has proved prohibitive
for widespread general application in ecological studies.
Other radioactive alternatives besides water, such as rubid-
ium, have also been tested, but their use has been contested
due to ethical reasons (Tomlinson et al., 2014). Regardless of
the technique used, isotope measurements require repeated
capture of individuals, which is a factor that risks disturbing
movement behaviours of targeted individuals.
Biologgers and biotelemetry
With the advent of internal temperature and heart rate log-
gers, it is possible to correlate changes in observed movement
behaviours with an animal’s metabolic rate (Cooke et  al.,
2004; Green et al., 2009). By inserting a sensor device within
an animal at a location close to the heart or a blood vessel,
both body temperature and heart rate can be recorded con-
tinuously at high frequencies (Bolen et  al., 2005; Ropert-
Coudert and Wilson, 2005; Wilson et al., 2006; Signer et al.,
2010). The data are recorded continuously by an on-board
logger (biologger) or transmitted (biotelemetry), without a
need for short-term recapture of the individual.
The rapid growth of biologger and biotelemetry technology
over the past several decades has improved our ability to evalu-
ate the physiological cost of different movement behaviours.
Progress in biotelemetry and the development of biologgers
began mostly in marine systems, where it has been difficult to
obtain information about the animals in other ways (Ropert-
Coudert and Wilson, 2005). For example, Bevan et al. (1995), in
a study of black-browed albatrosses (Diomedea melanophris),
measured both abdominal temperature and heart rate and
reported significant variations in energy expenditure during dif-
ferent behaviours and stages of the reproductive cycle. Likewise,
biotelemetry tags implanted into the swimming musculature of
migratory Fraser River sockeye salmon (Oncorhynchus nerka)
cannot only provide a measure of locomotor activity, but once
calibrated, can be used to estimate the energetic cost of migra-
tion (Cooke et al., 2008; Wilson et al., 2015).
Biologgers have also proved particularly useful for moni-
toring energetic costs of behaviours that were otherwise dif-
ficult to detect through movement data alone. For example,
although Cocherell et al. (2011) observed minimal upstream
or downstream movements by rainbow trout (Oncorhynchus
mykiss) in response to pulsed water flows from a hydroelectric
dam, use of biosensor tags revealed that they generally exhibit
increased energetic output and decreased foraging opportuni-
ties. While additional investigations into the potential longer-
term consequences and conservation implications are needed,
this study illustrates the value of accounting for physiology
Review article
when assessing the movement ecology of species. Overall,
with the development of smaller and longer-lasting biologger
and biotelemetry devices (allowing for their implementation
across a wide range of taxa) that can record multiple variables
simultaneously and transmit remotely, this area offers one of
the most exciting and rapidly growing techniques in the study
of animal movement physiology (Cooke et al., 2004; Bolen
et al., 2005; Bogard et al., 2010; Wilson et al., 2015).
Nutrition
Meeting dietary and nutritional needs can also be an internal
physiological factor driving animal movement behaviours.
Water is a key limiting compound for almost all terrestrial ver-
tebrates, influencing their movement path decisions and lon-
ger-term patterns in animal spatial ecology (Redfern et  al.,
2003). In addition, demand for other key limiting nutrients
often drives movement decisions in complex and interactive
ways. For example, Ortiz-Maciel et al. (2010) observed that
variation in movement and space use patterns by maroon-
fronted parrots (Rhynchopsitta terrisi) was likely to be a com-
plex interaction of reproductive state, food availability and the
location of clay licks that contain salt and other key nutrients
(Emmons and Stark, 1979; Powell et al., 2009). Further­more,
once key limiting nutrients are identified, resource managers
can manipulate their availability to modify animal movement
and migration (Sahlsten et al., 2010; Jones et al., 2014).
Investigation of the relationship between animal nutrition
and movement is most easily accomplished by simultaneous
monitoring of foraging and movement behaviour or by retro-
spective analyses of nutrition combined with tracking data
(Giroux et al., 2012). At a fine spatial scale, focal monitoring
of movement and foraging activity can be combined to relate
movement to nutritional intake. Likewise, forage intake and
behaviour can be estimated retroactively from evidence at a
kill or foraging site (Sand et al., 2005), analysis of faecal sam-
ple content (Munro et al., 2006) or measurement of stable
isotopes in blood or faecal samples (Vogel, 1978). Once these
types of data are collected, they can be linked retrospectively
with tracking data to provide information on the likely
energy expenditure and nutritional status of tracked individ-
uals during specific time periods (Hebblewhite et al., 2008).
Further­more, stable isotopes can be used to monitor for poten-
tially important carry-over effects of diet and nutrition
between life-history periods that are likely to influence vari-
ous processes, including movement behaviour (O’Connor
et al., 2014).
Measurements of body fat provide another important indi-
cation of an individual’s nutritional status. Body fat indices
offer a method of quantifying past energetic accumulation as
well as energy reserve potential (Robbins, 1983). For inverte-
brates, this is most easily achieved through molecular tech-
niques, such as the extraction and quantification of lipids
from migratory individuals sampled along their route (Brower
et al., 2006). For vertebrates, in addition to molecular tools,
ultrasonography and manual palpation can be used to
3

Review article
e­ stimate percentage body fat (Cooke et al., 2004; Cooke and
O’Connor, 2010), which can then be related to different life-
history parameters and to individual- and population-level
performance. These methods resemble the isotope method in
that the same individual needs to be recaptured to estimate the
relative gain or loss of body fat in a given time interval. For
example, Monteith et  al. (2011) related the tendency to
migrate in mule deer to the nutritional condition of the
females by measuring the ingesta-free body fat, which showed
that females in poorer condition were more likely to migrate.
Studies of birds also demonstrated distinct patterns, where
individuals in better condition after migration, as indicated by
fat reserves, were more likely to survive harsh weather periods
(Morrison et al., 2007). Finally, in addition to simultaneous
monitoring of movement behaviour and nutritional metrics,
the most promising area of research is in integrating these
metrics with monitoring of extrinsic or environmental condi-
tions. Findings that integrate across these data streams (e.g.
McWilliams et  al., 2004; Brower et  al., 2006; Middleton
et al., 2013) have transformed our understanding of a popula-
tion or species′ movement behaviour and will continue to
guide conservation.
Endocrinology
The endocrine system and its associated hormones control or
modulate physiological functions within the body. The rapidly
growing subject of field endocrinology is likely to be of particu-
lar interest to movement ecologists because of its focus on the
hormonal drivers that often serve as mechanisms underlying
observed behavioural responses to environmental challenges
(Walker et al., 2005). For instance, it is widely apprec­iated that
release of stress hormones is the physiological mechanism that
facilitates an adaptive response by an individual following
exposure to a stressor. Resultant movement behaviours include
long-distance dispersal or restricted movements that are indica-
tive of refuge behaviour (Wingfield and Romenofsky, 1997;
Jachowski et al., 2012, 2013a). Thus, knowledge of hormonal
control mechanisms is important not only for correct identifica-
tion of the baseline physiological state of an organism, but
also  for understanding how it responds to variation in its
­environment.
Three specific types of hormones and their associated func-
tions are currently of most interest to movement ecologists.
First, as mentioned above, measurement of glucocorticoid
stress hormones (cortisol and corticosterone) is often used to
quantify the effect of chronic or acute stressors on an individ-
ual or population (Millspaugh and Washburn, 2004).
Glucocorticoids released by the hypothalamic–pituitary–adre-
nal axis after exposure to a stressor interact with internal
receptors to facilitate the direction and prioritization of energy
to different processes within the organism (McEwen and
Wingfield, 2003; Romero and Butler, 2007). Concentrations of
these hormones can be monitored by invasive sampling (by
blood, saliva or urine collection) or by non-invasive extraction
of hormones from hair, feathers or faeces (Millspaugh and
Washburn, 2004; Walker et  al., 2005). Regardless of the
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Conservation Physiology • Volume 3 2015
s­ampling technique, all approaches must be validated, and
some sort of physiological baseline or basal physiological state
must be established with which to compare subsequent sam-
ples (Millspaugh and Washburn, 2004). Finally, in order to
integrate data on circulating stress hormone concentrations
with movement data effectively, it is important to determine
what is causing the stress response so that appropriate external
factors are considered in building models of animal movement.
A second important use of hormonal monitoring in animal
movement is to discern the reproductive state of an individ-
ual. At the population level, many animal species undertake
seasonal migrations to areas that serve as breeding or natal
areas, the timing of which is known to vary based on physi-
ological conditions (Newton, 2010). Even for species that do
not exhibit such distinct migration periods, differences in
movement exist based on reproductive state. For example, in
male African elephants (Loxodonta africana), the sampling
of testosterone provides valuable insight into when individu-
als are in musth and can be expected to vary in their move-
ment behaviours (Poole, 1987; Whitehouse and Schoeman,
2003). Movement behaviours can also vary in females based
on their reproductive state (Singh and Ericsson, 2014). For
example, female moose exhibit restricted movements and
select areas of dense cover during parturition (Bowyer et al.,
1999). Unfor­tunately, there are few direct studies addressing
the role of oestrogen hormone concentrations on animal
movement in a field setting and those that do exist show less
clear correlative trends with movement behaviour in com-
parison to testosterone (Cooke et al., 2006). However, lim-
ited information from observational field studies suggests
that elevated concentrations of oestrogens are likely to play a
mechanistic role in animal behaviour and spatial ecology. For
example, Wasserman et al. (2012) found that the consump-
tion of plants that produce oestrogen-mimicking compounds
was correlated with increased copulation and territoriality in
red colobus monkeys (Procolobus rufomitratus). The poten-
tial hormonal mechanisms underlying dispersal decisions by
individual animals, which can be highly variable and not
based solely on external factors, are in need of further
research (Paradis et al., 1998). Thus, while further research
into the role of androgens and oestrogens in movement
behaviour of free-ranging animals is needed, it is clear that
these hormones are not only associated with reproductive
state, but that they are also likely to have a mechanistic role
in movement behaviour.
Melatonin, produced by the pineal gland, represents a third
major type of hormone of potential importance to movement
ecologists owing to its role in control of circadian rhythms
(Cassone and Menaker, 1984). A majority of research on the
role of melatonin in movement decisions has focused on pas-
serine birds, in which melatonin concentrations have been
shown to differ seasonally based on changes in day length
(Gwinner et al., 1993; Fusani and Gwinner, 2005). Increases
in melatonin concentrations during migration have been
linked to the timing of migration (Schneider et  al., 1994;
Fusani and Gwinner, 2004), as well as the increased ability to
Conservation Physiology • Volume 3 2015
orient during migration (Cooke et al., 2008). There has been
little further work on the role played by melatonin in move-
ment decisions by other migratory species.
Immunology and ecotoxicology
Disease and toxic agents can have direct impacts on the fitness
and movement behaviour of animals. Diseases are known not
only to impact overall fitness of an individual and limit its abil-
ity to move, but also to alter the movements and behaviour of
infected individuals (Moore, 1995; Poulin, 2000, 2010; Klein
et al., 2004). One of the more interesting examples comes from
the protozoan parasite, Toxoplasma gondii, which reverses the
innate aversion of rats (Rattus spp.) to cat (Felis catus) odour,
causing cat odour to be an attractant to rats and allowing the
parasite to reach its definitive host, the cat (Berdoy et  al.,
2000). Furthermore, even the risk of encountering parasites
and infectious agents can influence animal movement behav-
iours, such as the bunching of herd animals and selection of
habitats based on avoidance of insect pests (Rutberg, 1987;
Mooring and Hart, 1992).
Exposure to toxicants also can contribute to observed
variation in movement patterns in obvious and subtle ways.
The exposure to external contaminants, such as oils and
detergents, can impact thermoregulation and movement
capacity of birds and terrestrial animals (Stephenson, 1997).
Internally, contaminants not only provide a potential limit to
fitness, leading to disease-related concerns, but also can influ-
ence physiological processes important to animal movement.
For example, elevated concentrations of mercury in fish and
wildlife can impair neurological and endocrine functions
(Eisler, 2006; Franceschini et al., 2008; Wada et al., 2009),
probably influencing hormone-modulated movement behav-
iours as well as cognitive processes, such as navigational
capacity.
While some indices of epidemiological state and toxico-
logical burden can be detected by external features (e.g. facial
tumours, oiling, etc.), physiological measures provide a more
robust assessment that can often be integrated simultane-
ously with other physiological measures. Disease surveillance
is primarily accomplished through blood-based assays for
blood-borne pathogens or titres produced as part of the
immune response (Artois et al., 2009). Likewise, toxicologi-
cal burdens can often be quantified through the blood, and in
some cases non-invasively through faeces, saliva and epider-
mis (skin, nails, etc.; Elliott et al., 2011). Beyond what can be
inferred by measuring only the presence or absence of a dis-
ease or amount of a toxicological burden, we encourage
researchers to evaluate energetic and endocrine system func-
tions simultaneously in order to maximize the potential infer-
ence gained from invasive and non-invasive sampling. For
example, the use of biotelemetry simultaneously to assess
energetic state, disease status and movement behaviour offers
particularly exciting opportunities to gain new insights into
observed movement behaviour and disease ecology (Adelman
et al., 2014).
Review article
A framework for better linking animal
movement and physiology
As discussed in the preceding sections, there are multiple
examples that illustrate how researchers have successfully
integrated physiology into studies of animal movement.
Inclusion of physiological measurements not only comple-
ments field studies of animal movement, but in some cases
reveals hidden costs or consequences not apparent by assess-
ment of spatial movement data alone (e.g. Walker et al., 2005;
Cocherell et al., 2011). Furthermore, as discussed by Lennox
et al., 2015, such findings have greatly advanced our under-
standing of migration. However, we feel that broader integra-
tion of physiological metrics to develop a greater
understanding of animal movement has been limited up to
this point, owing in part to the lack of a conceptual frame-
work governing how to integrate these measures in practice.
Nathan et al. (2008), in their initial description of a concep-
tual framework for the field of movement ecology (which they
describe as being composed of external factors, internal state,
navigation capacity and motion capacity), define internal state
as a term that accounts for the physiological (and perhaps psy-
chological) state ‘driving the organism to fulfill one or more
goals’. They go on to describe various goals of gaining energy,
seeking safety, reproduction and other phenomena as exam-
ples of how, as a field, ‘internal state consists of a multidimen-
sional vector of many states’. Clearly, ‘internal state’ has been
used as an umbrella term for a number of internal characteris-
tics. However, we feel that internal state requires a more
nuanced redefinition based on recent advances and the need
for more pragmatic guidance on how to quantify and integrate
measurements of internal state into movement ecology.
The mechanisms that drive the movement of an individual
or population are best viewed in an evolutionary context, in
which species have evolved life-history strategies that include
physiological adjustments that are a key element of animal
plasticity. Physiological control mechanisms dictate how an
animal exhibits sufficient phenotypic plasticity during its life
to maintain fitness (Ricklefs and Wikelski, 2002). Thus, in
order to understand variation in movement patterns and
address the question of why animals move the way they do,
we need to understand how physiological control mechanisms
constrain and dictate variation in how an individual responds
to its surrounding environment (Cooke et al., 2008, 2012).
Accordingly, within the conceptual framework of move-
ment ecology, we suggest that the term ‘internal state’ be aban-
doned in favour of the more accurate term ‘physiological state’.
Similar to the movement ecology paradigm put forth by
Nathan et al. (2008) involving internal state, we propose that
physiological state should be one of the primary fields of inves-
tigation in movement ecology, where observed movement
behaviours operate at the intersection of physiological state,
navigational capacity, motion capacity and external factors
(Fig. 1). However, in contrast to previous frameworks, we pro-
pose that physiological state plays an important mechanistic
5

Review article Conservation Physiology • Volume 3 2015

Figure 1:  A proposed revised conceptual framework for investigations into animal movement ecology (adapted from Nathan et al. 2008), which
depicts how movement behaviour of an individual is a function of two distinct phases. First (A), we propose that an animal is motivated or driven
to move as a result of its internal physiological state as well as proximate external cues. Second (B), the movement path taken by an individual is
modulated or influenced by a complex interaction of physiological state and external environment, as well as by motion and navigational
capacity.

role in movement behaviour that can best be investigated in
two phases or stages. First, we propose that physiological mea-
sures be investigated and considered along with external cues
as proximate drivers of an individual’s decision to move
(Fig. 1). The driving role played by physiology and external
conditions in the decision to move is a relatively well-estab-
lished relationship in ectothermic animals for thermoregula-
tion (Angilletta et  al., 2009; Sears and Angilletta, 2015).
Similar patterns are evident in some endotherms, where Signer
et al. (2010) have demonstrated that alpine ibex (Capra ibex)
migrate across an elevational gradient to facilitate digestion by
increasing their rumen temperature (i.e. hypermetabolism).
Furthermore, across a range of vertebrate and invertebrate
­species, physiology is more broadly documented as a key driver
in the timing of migratory movements (Lennox et al., 2015).
Second, in addition to driving the decision to move, physi-
ological state clearly interacts in complex ways with external
environmental conditions to modulate animal movement
behaviour along a movement track (Fig. 1). While less com-
monly studied in comparison to the driving role played by
physiology in movement, this area of work has great potential
to inform our understanding of movement behaviour. For
example, real-time GPS tracking of African elephants has been
combined with non-invasive sampling of stress hormones to
reveal complex movement path decisions related to glucocor-
ticoid concentrations and refugia or stopover use, corridor use
and streaking behaviour (i.e. rapid unidirectional movement
along a corridor; Jachowski et al., 2012, 2013a, b). Thus, the
extent to which an animal revisits or avoids a particular site
along a movement track is based on its past experiences with
external factors at that site and its ability to navigate toward
or away from it and is modulated by physiological condition.
Better integration of physiological measures within our
framework can also improve our understanding of complex
phenomena that modulate movement patterns, such as mem-
ory and learning. For example, toxic concentrations of mer-
cury have been shown to impair hormone-modulated
movement behaviours and navigational capacity (Stephenson,
1997; Eisler, 2006). Thus, while the concepts of memory and
learning in movement ecology have been difficult to quantify
and somewhat controversial (such as the topic of cognitive
maps; Bennett, 1996; Mueller and Fagan, 2008), under our

6
Conservation Physiology • Volume 3 2015
framework we encourage further research on how memory in
free-ranging animals can be investigated as a separate cogni-
tive process based on the intersection of physiological state,
external factors and navigational capacity.
Current limitations and recommenda-
tions for future research
Despite progress and developments in the measurement of the
physiological state of free-ranging animals, and a framework
for incorporating those measures as summarized above, it is
important to acknowledge current limitations and areas in
need of further research. A number of concerns remain about
the assumptions, applicability, scale, technical capability, ani-
mal welfare and cost issues associated with current methods
used to measure physiological state in animals. Furthermore,
in addition to the need for methodological advancements,
theoretical advancements will be needed to provide better
integration of measures of physiological state into studies of
animal movement. In this section, we discuss these issues and
attempt to lay the path of future progress in the field.
Limitations and assumptions of current
techniques
One of the first issues that should be addressed when attempt-
ing to monitor physiological state is the reliability of these
methods in what they measure. Each technique comes with
unique assumptions, costs and benefits and is subject to criti-
cism. For example, Butler et al. (2004) reviewed the advan-
tages and disadvantages of DLW and heart rate methods and
found that the biotelemetry methods have a great potential,
especially due to their accuracy and versatility. Furthermore,
DLW techniques typically make several common assumptions
that deserve additional evaluation, such as the following:
(i) rate of flow of materials and size of the body are constant
throughout the temporal scale of measurement; (ii) all materi-
als leaving the body take isotopes with them at a similar rate
to body water; and (iii) hydrogen and oxygen atoms only take
part in reactions that involve water and CO2, and spent iso-
topes do not re-enter the body (Nagy and Costa, 1980;
Speakman, 1997; Tomlinson et al., 2014). Measures of heart
rate, respiratory rate and body temperature also involve
assumptions because they assess only some of the many phys-
iological factors that influence metabolic rate (Cooke et al.,
2004; Green, 2011). Thus, while logistical constraints often
drive sampling methodologies in field-based studies, it is also
important to be aware of the assumptions and biases inherent
in each technique.
A second critical issue is to establish what the physiological
metrics being collected genuinely represent. Physiological
state metrics can vary greatly among techniques, as well as
among individual animals, populations and species (Sheriff
et al., 2011). Thus, it is necessary to consider not only the
logistical constraints and the validity of measurements, but
also what those values mean to the individual or population.
Review article
It is for this reason that most physiological studies of wildlife
are based on comparisons of measurements collected before
and after experimental treatment or exposure to a discrete
environmental stressor (Wingfield et al., 1997). In this way,
researchers can establish a baseline with which to compare the
physiological response of an individual or set of individuals
post-treatment. Likewise, in the study of wild animals, where
experimental manipulation might not be possible, it is critical
to establish a physiological baseline with which to compare
subsequent measurements. This can be accomplished by com-
parisons with captive populations or other wild populations,
but it is ideally based on individual physiological metrics prior
to a movement activity or exposure to a stressor, taking into
account seasonal and daily rhythms that are often inherent in
physiological state metrics (Millspaugh and Washburn, 2004).
Following on the issue of what a specific physiological met-
ric represents, there is the question of how representative it is
of the individual, population or species. Similar to other fields
of ecological inquiry, researchers must think critically about
issues of spatial and temporal scale when sampling physiolog-
ical state. A spatially balanced sampling design should be
devised to enable accounting for individual, population or
species-specific variability. Temporally, because most direct
measures of physiological state require repeated capturing of
individuals, most physiological measures are limited to peri-
ods of time between or immediately preceding sampling
events. For many free-ranging animals, the difficulty of reli-
ably capturing them and the limitation of inference to a spe-
cific window of time might make direct measurement of
physiological state unsuitable as a method. While repeated
captures or attached biologgers can assist in expanding the
temporal period of inference, the benefits of such techniques
should be balanced with concerns about the resulting distur-
bance to the animal (White et al., 2013).
Animal welfare and non-invasive sampling
The rapid proliferation of techniques to monitor the physio-
logical state of animals involves both invasive and non-­
invasive techniques that bring up important animal welfare
concerns. Historically, most techniques required repeated cap-
ture and handling that, at a minimum, momentarily influence
animal movement and, in some cases, can have prolonged
negative impacts. For example, the recent use of radioactive
isotopes, such as rubidium, has been shown to track field met-
abolic rate reliably, but it has clear animal welfare and toxico-
logical implications (Tomlinson et al., 2013). Biologgers offer
a tremendous tool for intensively monitoring the physiologi-
cal state of an organism over an extended period of time, but
similar to other attached tracking devices, they must be evalu-
ated carefully so as not to impact movement behaviours or
otherwise negatively affect marked individuals (Authier et al.,
2013; Thomson and Heithaus, 2014). These concerns high-
light the value of non-invasive sampling of faeces, hair and
other materials for certain direct and indirect physiological
measures. Rapid advances in such techniques make them
increasingly valuable tools for gathering reliable metrics of
7

Review article
animal physiology with little or no disturbance to the animal.
However, this benefit must be weighed against the difficulty of
discerning the period of time represented by the sample, as
well as the identity of the individual sampled, both of which
can be critical to interpretation of results and subsequent
inference (Goyman, 2012; Jachowski et  al., 2013a). Thus,
while certain measures of animal physiology will continue to
require animal capture, less invasive (such as self-detaching
collars) and non-invasive technologies are rapidly advancing
that minimize animal welfare concerns.
Establishment of indirect measures of
physiological state
In general, the monitoring of physiological state in a field set-
ting is likely to take one of the following two forms: (i) fine-
scale simultaneous tracking of individual animal movements
and physiological state that allows for comparisons in move-
ment and physiological correlates over time and across geo-
graphical gradients; or (ii) comparative studies of movement
behaviours between animals or populations categorized as
being in different physiological states. Across both approaches,
as mentioned above, a key limitation of many techniques is the
need to capture individuals repeatedly in order to measure and
assess physiological state. However, once a basic understand-
ing of physiological state is developed, more easily detected
indirect measures of physiological state can be used in some
scenarios. For example, once a fundamental understanding of
the hormonal rhythms of males and females during reproduc-
tive periods is understood, physiological state can sometimes
be generalized for specific individuals, populations or species
based on time of year or visual observation (Jainudeen et al.,
1972). Likewise, visual observation of diseased individuals or
those carrying a toxic burden can be integrated into studies of
movement ecology once direct physiological monitoring is
undertaken to validate such gross categorizations.
Inference of physiological state based on movement path
or body accelerometry is increasingly common in movement
ecology (Brown et al., 2013). In the emerging field of dynamic
accelerometry, the assumption that movement requires energy
serves as a basis for the modelling of energy expenditure based
on movement behaviours (Green et al., 2009; Wilson et al.,
2011). Developing a more nuanced and broader understand-
ing of energy flow across space and time allows for the devel-
opment of ‘energy landscape’ models in the study of animal
movement (Shepard et al., 2013). However, we again caution
that such assumptions must first be evaluated through rigor-
ous direct sampling of physiological state to obtain corrobo-
rative evidence that such an energetic relationship exists for a
given species and to identify other factors that are likely to
contribute to energetic state (Halsey et al., 2011). Likewise, a
ripe area for further research is the correlation between move-
ment path characteristics or body accelerometry and endo-
crine system functions (Jachowski et  al., 2013a). Once
hormone sampling and assay techniques (such as faecal radio-
immunoassays) are validated and measured for a species in a
8
Conservation Physiology • Volume 3 2015
field setting, it might be possible to discern physiological state
indirectly through movement behaviours.
Conclusion
Collectively, it is evident that studies of animal movement can
be advanced greatly by better integration of measures of physi-
ological state. Rapid advances over the past several decades
have made a wide variety of tools available to measure the phys-
iological state of free-ranging animals. Conceptually, we pro-
pose that these physiological measures should be investigated as
both drivers and modulators of movement (Fig. 1). To achieve
this in practice, researchers must proceed on two key fronts.
First, research should be directed at discerning basic, predictable
biorhythms of a species (e.g. energetic needs, reproductive tim-
ing). This can be viewed as a type of physiological baseline or
envelope within which an individual typically operates. Second,
research is needed to evaluate how physiological control mech-
anisms can influence an individual’s response to disturbances or
change and to enable a distinction to be made between the
responses generated by different extrinsic conditions.
A major theme from our review is the need to integrate
multiple measures or streams of data (e.g. reproductive status,
energy expenditure, ambient temperature) to improve our
understanding of relatively complex movement behaviours,
such as migration. Undertaking such interdisciplinary investi-
gations will not only help lead to a more mechanistic under-
standing of animal movement behaviour, but also allow us to
improve our ability to predict how species are likely
to respond to perturbations in a rapidly changing world and
to develop appropriate conservation strategies.
Acknowledgements
We thank R. Jachowski, R. Nathan, S. Cooke and two anony-
mous reviewers for helpful comments that improved this
manuscript.
References
Adelman JS, Moyers SC, Hawley DM (2014) Using remote biomonitoring
to understand heterogeneity in immune-responses and disease-
dynamics in small, free-living animals. Integr Comp Biol 54: 377–386.
Angilletta MJ, Sears MW, Pringle RM (2009) Spatial dynamics of nesting
behavior: lizards shift microhabitats to construct nests with benefi-
cial thermal properties. Ecology 90: 2933–2939.
Artois M, Bengis R, Delahay RJ, Duchêne MJ, Duff JP, Ferroglio E, Gortaxar
C, Hutchings MR, Kock RA, Leighton FA et al. (2009) Wildlife disease sur-
veillance and monitoring. In Delehay RJ, Smith GC, Hutchings MR, eds,
Management of Disease in Wild Mammals. Springer, Japan, pp 187–213.
Authier M, Péron C, Mante A, Vidal P, Grémille D (2013) Designing obser-
vational biologging studies to assess the causal effect of instrumen-
tation. Methods Ecol Evol 4: 802–810.
Conservation Physiology • Volume 3 2015 Review article

Bennett AT (1996) Do animals have cognitive maps? J Exp Biol 199: 219–224. ology in practice: how physiological knowledge has improved our
ability to sustainably manage Pacific salmon during up-river migra-
Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats
tion. Philos Trans R Soc Lond B Biol Sci 367: 1757–1769.
infected with Toxoplasma gondii. Proc Biol Sci 267: 1591–1594.
Eisler R (2006) Mercury Hazards to Living Organisms. Taylor and Francis
Bevan RM, Butler PJ, Woakes AJ, Prince PA (1995) The energy expenditure
Publishers, London.
of free-ranging black-browed albatrosses. Philos Trans R Soc B 350:
119–131. Elliott JE, Bishop CA, Morrissey CA (2011) Wildlife ecotoxicology: forensic
approaches. In Elliott JE, Bishop CA, Morrissey CA, eds, Wildlife
Bogard SJ, Block BA, Costa DP, Godley BJ (2010) Biologging technologies:
Ecotoxicology: Forensic Approaches. Springer, New York, pp 1–9.
new tools for conservation. Endangered Species Res 10: 1–7.
Emmons LH, Stark NM (1979) Elemental composition of a natural mineral
Bolen MS, Cochran WW, Wikelski MC (2005) Biotelemetry of new world
lick in Amazonia. Biotropica 11: 311–313.
thrushes during migration: physiology, energetics and orientation in
the wild. Integr Comp Biol 45: 295–304. Franceschini MD, Custer CM, Custer TW, Reed JM, Romero LM (2008)
Corticosterone stress response in tree swallows nesting near poly-
Bowlin MS, Bisson IA, Shamoun-Baranes J, Reichard JD, Sapir N, Marra PP,
chlorinated biphenyl- and dioxin-contaminated rivers. Environ
Kunz TH, Wilcove DS, Hedenström A, Guglielmo CG et al. (2010)
Toxicol Chem 11: 2326–2331.
Grand challenges in migration biology. Integr Comp Biol 50: 261–279.
Fryxell JM, Sinclair ARE (1988) Causes and consequences of migration by
Bowyer RT, Van Ballenberghe V, Kie JG, Maier JA (1999) Birth-site selec-
large herbivores. Trends Ecol Evol 3: 237–241.
tion by Alaskan moose: maternal strategies for coping with a risky
environment. J Mammal 80: 1070–1083. Fusani L, Gwinner E (2004) Simulation of migratory flight and stopover
affects night levels of melatonin in a nocturnal migrant. Proc Biol Sci
Brower LP, Fink LS, Walford P (2006) Fueling the fall migration of the mon-
271: 205–211.
arch butterfly. Integr Comp Biol 46: 1123–1142.
Fusani L, Gwinner E (2005) Melatonin and nocturnal migration. Annu Rev
Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP (2013) Observing the
NY Acad Sci 1046: 264–270.
unwatchable through acceleration logging of animal behavior. Anim
Biotelem 1: 20. Getz WM, Saltz D (2008) A framework for generating and analyzing
movement paths on ecological landscapes. Proc Natl Acad Sci USA
Butler PJ, Green JA, Boyd IL, Speakman JR (2004) Measuring metabolic
105: 19066–19071.
rate in the field: the pros and cons of the doubly labelled water and
heart rate methods. Funct Ecol 18: 168–183. Giroux MA, Berteaux D, Lecomte N, Gauthier G, Szor G, Bêty J (2012)
Benefiting from a migratory prey: spatio-temporal patterns in alloch-
Cassone VM, Menaker M (1984) Is the avian circadian system a neuroen-
thonous subsidization of an arctic predator. J Anim Ecol 81: 533–542.
docrine loop? J Exp Zool 232: 539–549.
Goyman W (2012) On the use of non-invasive hormone research in
Cocherell SA, Cocherell DE, Jones GJ, Miranda JB, Thompson LC, Cech JJ,
uncontrolled, natural environments: the problem with sex, diet,
Klimley AP (2011) Rainbow trout Oncorhynchus mykiss energetic
metabolic rate and the individual. Methods Ecol Evol 3: 757–765.
responses to pulsed flows in the American River, California, assessed
by electromyogram telemetry. Environ Biol Fish 90: 29–41. Green JA (2011) The heart rate method for estimating metabolic rate:
review and recommendations. Comp Biochem Physiol A Mol Integr
Cooke SJ, O’Connor CM (2010) Making conservation physiology relevant to
Physiol 158: 287–304.
policy makers and conservation practitioners. Conserv Lett 3: 159–166.
Green JA, Halsey LG, Wilson RP, Frappell PB (2009) Estimating energy expen-
Cooke SJ, Hinch SG, Wikelski M, Andreas RD, Kuchel LJ, Wolcott TG, Butler
diture of animals using the accelerometry technique: activity, inactivity
PJ (2004) Biotelemetry: a mechanistic approach to ecology. Trends
and comparison with the heart rate technique. J Exp Biol 212: 471–482.
Ecol Evol 19: 334–343.
Gwinner E, Schwabl-Benzinger I, Schwabl H, Dittami J (1993) Twenty-four
Cooke SJ, Hinch SG, Crossin GT, Patterson DA, English KK, Healey MC,
hour melatonin profiles in a nocturnally migrating bird during and
Shrimpton JM, Van Der Kraak G, Farrell AP (2006) Mechanistic basis of
between migratory seasons. Gen Comp Endocrinol 90: 119–124.
individual mortality in Pacific salmon during spawning migrations.
Ecology 87: 1575–1586. Halsey LG, Shepard ELC, Wilson RP (2011) Assessing the development and
application of the accelerometry technique for estimating energy
Cooke SJ, Hinch SG, Farrell AP, Patterson DA, Miller-Saunders K, Welch
expenditure. Comp Biochem Physiol A Mol Integr Physiol 158: 305–314.
DW, Donaldson MR, Hanson KC, Crossin GT, Mathes MT et al. (2008)
Developing a mechanistic understanding of fish migrations by link- Hambly C, Voigt C (2011) Measuring energy expenditure in birds using
ing telemetry with physiology, behavior, genomics and experimental bolus injections of 13C-labelled Na-bicarbonate. Comp Biochem
biology: an interdisciplinary case study on adult Fraser River sockeye Physiol A Mol Integr Physiol 258: 323–328.
salmon. Fisheries 33: 321–338.
Hebblewhite M, Merrill E, McDermid G (2008) A multi-scale test of the
Cooke SJ, Hinch SG, Donaldson MR, Clark TD, Eliason EJ, Crossin GT, Raby forage maturation hypothesis in a partially migratory ungulate pop-
GD, Jeffries KM, Lapointe M, Miller K et al. (2012) Conservation physi- ulation. Ecol Monogr 78: 141–166.

9

Review article
Holyoak M, Casagrandi R, Nathan R, Revilla E, Spiegel O (2008) Trends
and missing parts in the study of movement ecology. Proc Natl Acad
Sci USA 105: 19060–19065.
Isaac NJB, Carbone C, McGill B (2012) Population and community ecology.
In Sibly RM, Browh JH, Kodric-Brown A, eds, Metabolic Ecology: A
Scaling Approach. Wiley-Blackwell, London, pp 77–85.
Jachowski DS, Slotow R, Millspaugh JJ (2012) Physiological stress and
refuge behavior by African elephants. PLoS ONE 7: e31818.
Jachowski DS, Slotow R, Montgomery RA, Millspaugh JJ (2013a)
Unravelling complex associations between physiological state and
movement in African elephants. Funct Ecol 27: 1166–1175.
Jachowski DS, Slotow R, Millspaugh JJ (2013b) Corridor use and streak-
ing behavior by African elephants in relation to physiological state.
Biol Conserv 167: 276–282.
Jainudeen MR, Katongole CB, Short RV (1972) Plasma testosterone levels
in relation to musth and sexual activity in the male Asiatic elephant,
Elephas maximus. J Reprod Fertil 29: 99–103.
Jones JD, Kauffman MJ, Monteith KL, Scurlock BM, Albeke SE, Cross PC
(2014) Supplemental feeding alters migration of a temperate ungu-
late. Ecol Appl 24: 1769–1779.
Klein SL, Zink MC, Glass GE (2004) Seoul virus infection increases aggres-
sive behaviour in male Norway rats. Anim Behav 67: 421–429.
Lennox RJ, Chapman J, Souliére C, Tudorache C, Wikelski M, Metcalfe J,
Cooke SJ (2015) Conservation physiology in animal migration.
Conserv Physiol, in press.
Louzao M, Wiegand T, Bartumeus F, Weimerskirch H (2014) Coupling
instantaneous energy-budget models and behavioural mode analy-
sis to estimate optimal foraging strategy: an example with wander-
ing albatrosses. Mov Ecol 2: 8.
Lundberg J, Moberg F (2003) Mobile link organisms and ecosystem func-
tioning: implications for ecosystem resilience and management.
Ecosystems 6: 87–98.
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and
biomedicine. Horm Behav 43: 2–15.
McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting,
and feeding in birds during migration: a nutritional and physiologi-
cal ecology perspective. J Avian Biol 35: 377–393.
Meier AH, Farner DS, King JR (1965) A possible endocrine basis for migra-
tory behaviour in the white-crowned sparrow, Zonotrichia leucophrys
gambelii. Anim Behav 13: 453–465.
Middleton AD, Kauffman MJ, McWhirter DE, Cook JG, Cook RC, Nelson
AA, Jimenez MD, Klaver RW (2013) Animal migration amid shifting
patterns of phenology and predation: lessons from a Yellowstone elk
herd. Ecology 94: 1245–1256.
Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticoid metab-
olite measures in conservation biology research: considerations
for application and interpretation. Gen Comp Endocrinol 138:
189–199.
10
Conservation Physiology • Volume 3 2015
Monteith KL, Bleich VC, Stephenson TR, Pierce BM, Conner MM, Klaver
RW, Bowyer RT (2011) Timing of seasonal migration in mule deer:
effects of climate, plant phenology, and life-history characteristics.
Ecosphere 2: art47.
Moore J (1995) The behavior of parasitized animals. BioScience 45: 89–96.
Mooring MS, Hart BL (1992) Animal grouping for protection from parasites:
selfish herd and encounter-dilution effects. Behaviour 123: 173–193.
Morales JM, Haydon DT, Friar J, Holsinger KE, Fryxell JM (2004) Extracting
more out of relocation data: building movement models as mixtures
of random walks. Ecology 85: 2436–2445.
Morrison GRI, Davidson NC, Wilson JR (2007) Survival of the fattest: body
stores on migration and survival in red knots Calidris canutus island-
ica. J Avian Biol 38: 479–487.
Mueller T, Fagan WF (2008) Search and navigation in dynamic environ-
ments – from individual behaviors to population distributions. Oikos
117: 654–664.
Munro RHM, Nielsen SE, Price MH, Stenhouse GB, Boyce MS (2006)
Seasonal and diel patterns of grizzly bear diet and activity in west-
central Alberta. J Mammal 87: 1112–1121.
Nagy KA, Costa DP (1980) Water flux in animals: analysis of potential
errors in the tritiated water method. Am J Physiol Regul Integr Comp
Physiol 238: R454–R465.
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE
(2008) A movement ecology paradigm for unifying organismal
movement research. Proc Natl Acad Sci USA 105: 19052–19059.
Newton I (2010) The Migration Ecology of Birds. Academic Press, New York.
O’Connor CM, Norris DR, Crossin GT, Cooke SJ (2014) Biological carryover
effects: linking common concepts and mechanisms in ecology and
evolution. Ecosphere 5: art28.
Ortiz-Maciel SG, Hori-Ochoa C, Enkerlin-Hoeflich E (2010) Maroon-
fronted parrot (Rhynchopsitta terrisi) breeding home range and hab-
itat selection in the northern Sierra Madre Oriental, Mexico. Wilson J
Ornithol 122: 513–517.
Paradis E, Baillie SR, Sutherland WJ, Gregory RD (1998) Patterns of natal
and breeding dispersal in birds. J Anim Ecol 67: 518–536.
Patterson TA, Thomas L, Wilcox C, Ovaskainen O, Matthiopoulo J (2008)
State–space models of individual animal movement. Trends Ecol Evol
23: 87–94.
Poole JH (1987) Rutting behavior in African elephants: the phenomenon
of musth. Behaviour 102: 283–316.
Poulin R (2000) Manipulation of host behaviour by parasites: a weaken-
ing paradigm? Proc Biol Sci 267: 787–792.
Poulin R (2010) Parasite manipulation of host behavior: an update and
frequently asked questions. Adv Study Behav 41: 151–186.
Powell LL, Powell TU, Powell GV, Brightsmith DJ (2009) Parrots take it with
a grain of salt: available sodium content may drive collpa (clay lick)
selection in southeastern Peru. Biotropica 41: 279–282.
Conservation Physiology • Volume 3 2015
Pulido F (2007) Phenotypic changes in spring arrival: evolution, pheno-
typic plasticity, effects of weather and condition. Clim Res 35: 5–23.
Redfern JV, Grant R, Biggs H, Getz WM (2003) Surface-water constraints
on herbivore foraging in the Kruger National Park, South Africa.
Ecology 84: 2092–2107.
Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends
Ecol Evol 17: 462–468.
Robbins C (1983) Wildlife Feeding and Nutrition. Academic Press,
London, UK.
Romero LM, Butler LK (2007) Endocrinology of stress. Int J Comp Psychol
20: 85–95.
Ropert-Coudert Y, Wilson RP (2005) Trends and perspectives in animal-
attached remote sensing. Front Ecol Environ 3: 437–444.
Rutberg AT (1987) Horse fly harassment and the social behavior of feral
ponies. Ethology 75: 145–154.
Sahlsten J, Bunnefeld N, Månsson J, Ericsson G, Bergström R, Dettki H
(2010) Can supplementary feeding be used to redistribute moose?
Wildl Biol 16: 85–92.
Sand H, Zimmermann B, Wabakken P, Andrèn H, Pedersen HC (2005)
Using GPS technology and GIS cluster analyses to estimate kill rates
in wolf-ungulate ecosystems. Wildl Soc Bull 33: 914–925.
Sawyer H, Kauffman MJ (2011) Stopover ecology of a migratory ungu-
late. J Anim Ecol 80: 1078–1087.
Schick RS, Loarie SR, Colchero F, Best BD, Boustany A, Conde DA, Halpin
PN, Joppa LN, McClellan CM, Clark JS (2008) Understanding move-
ment data and movement processes: current and emerging direc-
tions. Ecol Lett 11: 1338–1350.
Schmidt-Nielsen K (1997) Animal Physiology: Adaptation and
Environment. Cambridge University Press, Cambridge.
Schneider T, Thalau HP, Semm P, Wiltschko W (1994) Melatonin is crucial
for the migratory orientation of pied flycatchers (Ficedula hypoleuca
Pallas). J Exp Biol 194: 255–262.
Sears MW, Angilletta MJ (2015) Costs and benefits of thermoregulation
revisited: both the heterogeneity and spatial structure of tempera-
ture drive energetic costs. Am Nat 185: E94–E102.
Shaffer SA (2011) A review of seabird energetics using doubly
labeled water method. Comp Biochem Physiol A Mol Integr Physiol
258: 315–322.
Shepard E, Wilson R, Quintana F, Gomez Laich A, Forman D (2009) Pushed
for time or saving on fuel: fine-scale energy budgets shed light on
currencies in a diving bird. Proc Biol Sci 276: 3149–3155.
Shepard EL, Wilson RP, Rees WG, Grundy E, Lambertucci SA, Vosper SB
(2013) Energy landscapes shape animal movement ecology. Am Nat
182: 298–312.
Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring
stress in wildlife: techniques for quantifying glucocorticoids.
Oecologia 166: 869–887.
Review article
Signer C, Ruf T, Schober F, Fluch G, Paumann T, Arnold W (2010) A versa-
tile telemetry system for continuous measurement of heart rate,
body temperature and locomotor activity in free-ranging ruminants.
Methods Ecol Evol 1: 75–85.
Singh NJ, Ericsson G (2014) Changing motivations during migration:
linking movement speeds to reproductive status in a migratory large
mammal. Biol Lett 10: 20140379.
Singh NJ, Grachev IA, Bekenov AB, Milner-Gulland EJ (2010) Saiga ante-
lope calving site selection is increasingly driven by human distur-
bance. Biol Conserv 143: 1770–1779.
Speakman J (1997) Doubly Labeled Water: Theory and Practice. Chapman
and Hall, London, UK.
Speakman JR (2005) The role of technology in the past and future devel-
opment of the doubly labelled water method. Isotopes Environ Health
Stud 41: 335–343.
Stephenson R (1997) Effects of oil and other surface-active organic pol-
lutants on aquatic birds. Environ Conserv 2: 121–129.
Thomson JA, Heithaus MR (2014) Animal-borne video reveals seasonal
activity patterns of green sea turtles and the importance of account-
ing for capture stress in short-term biologging. J Exp Mar Biol Ecol
450: 15–20.
Tomlinson S, Maloney SK, Withers PC, Voigt CC, Cruz-Neto AP (2013)
From doubly labelled water to half-life; validating radio-isotopic
rubidium turnover to measure metabolism in small vertebrates.
Methods Ecol Evol 4: 619–628.
Tomlinson S, Arnall SG, Munn A, Bradshaw SD, Maloney SK, Dixon KW,
Didham RK (2014) Applications and implications of ecological ener-
getics. Trends Ecol Evol 29: 280–290.
Urban M, Phillips BL, Skelly D, Shine R (2007) The cane toad’s (Chaunus
[Bufo] marinus) increasing ability to invade Australia is revealed by a
dynamically updated range model. Proc Biol Sci 274: 1413–1419.
Vogel JC (1978) Isotopic assessment of the dietary habits of ungulates. S
Afr J Sci 74: 298–301.
Wada H, Cristol DA, McNabb FA, Hopkins WA (2009) Suppressed adreno-
cortical responses and thyroid hormone levels in birds near a mer-
cury-contaminated river. Environ Sci Technol 43: 6031–6038.
Walker BG, Boersma PD, Wingfield JC (2005) Field endocrinology and
conservation biology. Integr Comp Biol 45: 12–18.
Ward S, Bishop CM, Woakes AJ, Butler PJ (2002) Heart rate and the rate of
oxygen consumption of flying and walking barnacle geese (Branta leu-
copsis) and bar-headed geese (Anser indicus). J Exp Biol 205: 3347–3356.
Wasserman MD, Chapman CA, Milton K, Gogarten JF, Wittwer DJ, Ziegler
TE (2012) Estrogenic plant consumption predicts red colobus mon-
key (Procolobus rufomitratus) hormonal state and behavior. Horm
Behav 62: 553–562.
White C, Cassey P, Schimpf N, Halsey L, Green J, Portugal S (2013)
Implantation reduces the negative effects of bio-logging devices on
birds. J Exp Biol 216: 537–542.
11

Review article
Whitehouse AM, Schoeman DS (2003) Ranging behaviour of elephants
within a small, fenced area in Addo Elephant National Park, South
Africa. Afr Zool 38: 95–108.
Wikelski M, Moskowitz D, Adelman JS, Cochran J, Wilcove DS, May ML
(2006) Simple rules guide dragonfly migration. Biol Lett 2: 325–329.
Wilcove DS, Wikelski M (2008) Going, going, gone: is animal migration
disappearing? PLoS Biol 6: e188.
Wilson ADM, Wikelski M, Wilson RP, Cooke SJ (2015) Utility of biological
sensor tags in animal conservation. Conserv Biol 29: 1065–1075.
Wilson RP, White CR, Quintana F, Halsey LG, Liebsch N, Martin GR, Butler
PJ (2006) Moving towards acceleration for estimates of activity-spe-
cific metabolic rate in free-living animals: the case of the cormorant.
J Anim Ecol 75: 1081–1090.
12
Conservation Physiology • Volume 3 2015
Wilson RP, Griffiths IW, Legg PA, Friswell MI, Bidder OR, Halsey LG, Shepart
ELC (2011) Turn costs change the value of animal search paths. Ecol
Lett 16: 1145–1150.
Wingfield JC, Romenofsky M (1997) Corticosterone and facultative dis-
persal in response to unpredictable events. Ardea 85: 155–166.
Wingfield JC, Schwabl H, Mattocks PW (1990) Endocrine mechanisms
of migration. In Winner E, ed., Bird Migration. Springer, Berlin, pp
232–256.
Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, Lepson J
(1997) Environmental stress, field endocrinology, and conservation
biology. In Clemmons JR, Buchholz R, eds, Behavioral Approaches to
Conservation in the Wild. Cambridge University Press, Cambridge, pp
95–131.